Agroforest Syst
https://doi.org/10.1007/s10457-018-0186-x
Effect of soil salinity on morphology and gas exchange
of two Paulownia hybrids
Katya Ivanova . Maria Geneva . Svetoslav Anev . Teodora Georgieva .
Nikolina Tzvetkova . Ira Stancheva . Yuliana Markovska
Received: 15 September 2016 / Accepted: 7 January 2018
Ó Springer Science+Business Media B.V., part of Springer Nature 2018
Abstract A pot experiment was carried out to
investigate the effect of salinity on growth, leaf
anatomy and gas exchange characteristics in two
Paulownia hybrid lines (Paulownia tomentosa 9 for-
tunei-TF and Paulownia elongata 9 elongata-T4).
The distribution of Mg, Ca, Na, K and Fe between
water available fractions from non-saline, saline soils,
and different organs showed acropetal concentration
gradient for metal accumulation, excepting Ca. Selec-
tive uptake of K over Na was enhanced slightly with
increasing salinity, where K/Na ratio was reduced in
Paulownia elongata 9 elongata-T4 and rose in
Paulownia tomentosa 9 fortunei-TF. The reduction
in the total plant leaf area and in the values of the
K. Ivanova
Y. Markovska
Department of Plant Physiology, Faculty of Biology,
University of Sofia, 8 Dragan Tsankov Blvd, 1164 Sofia,
Bulgaria
M. Geneva (&)
I. Stancheva
Department of Plant Soil Interactions, Institute of Plant
Physiology and Genetics, Bulgarian Academy of
Sciences, Acad. Georgi Bonchev str, bl. 21, 1113 Sofia,
Bulgaria
e-mail: boykova2@yahoo.com
S. Anev
N. Tzvetkova
Department of Plant Physiology, Faculty of Forestry,
University of Forestry, 10 Kliment Ochridski str,
1756 Sofia, Bulgaria
T. Georgieva
Biotree Ltd, 7 Shosse Bankya Str, 1080 Sofia, Bulgaria
intrinsic components of photosynthesis-maximal
Rubisco catalyzed carboxylation velocity, maximal
electron transport rate and triose phosphate utilization
rate was observed only in Paulownia tomen-
tosa 9 fortunei-TF. The CO2 compensation point
rose to Paulownia tomentosa 9 fortunei-TF and
declined in Paulownia elongata 9 elongata-T4,
while the stomatal factor values were enhanced in
both hybrid lines. Under saline conditions, the stom-
atal component was more limiting to photosynthesis
than its biochemical components. It was concluded
that Paulownia elongata 9 elongata-T4 was more
resistant to salinity because its growth and gas
exchange characteristics were less affected in com-
parison with Paulownia tomentosa 9 fortunei-TF.
Keywords A:Ci curves
Growth
Salinity
Introduction
Natural or primary salinity is more widespread in arid
and semi-arid regions of the world and results from the
accumulation of soluble salts in soils or groundwater
over long geological periods. Removal of water due to
evapotranspiration also leads to increased concentra-
tion of salts in the soil bioavailable fraction and excess
of sodium ions in the rhizosphere. Sodicity is a
secondary consequence of salinity, typical for clay
soils, where exchangeable sodium is bound to the
123

negative charges of clay. Besides the naturally-formed
saline and sodic soils, the occurrence of so-called
secondary salt-affected soils is due to the application
of different unsuitable agricultural practices and
continues to grow (Munns 2011). According to FAO
Land and Plant Nutrition Management Service, the
total surface of the saline regions of the world is the
almost 397 3 106 ha and 2% of them are secondary
salt-affected (Dajic 2006).
Salinity in soil or water is one of the major negative
influencing factors of the environment, and especially
in arid and semiarid regions, can severely limit crop
production. In recent decades, the investigations are
focused on biochemical and physiological traits
(Munns and Richards 2007; Koyro et al. 2014),
identification of key genes and/or discovering of
distinctive molecular markers in a great number of
agricultural crops (Kosova et al. 2011). Munns (2011)
proposed that increased salt tolerance of perennial
species (such as woody species) used for fodder or
biofuel production is a key component in reducing the
spread of secondary salinity, while increased salt
tolerance of crops will directly improve production in
soils with primary salinity.
Woody species from the genus Paulownia
(Paulowniaceae) is native from China. Paulownia
tomentosa as high-yielding plants (Woods 2008) can
be used for the production of energy, paper pulp, and
wooden building materials. Over the last two decades,
Paulownia species has been extensively studied due to
its ability to uptake heavy metals (Doumett et al.
2008, 2011; Wang et al. 2010; Madejon et al. 2016).
Paulownia tomentosa (Thunb.) Stend, as well as
other species, belong to the genus Paulownia (P.
elongata, P. fortunei) and hybrid (P. fortunei 9 to-
mentosa) are used for afforestation of Eastern Black
Sea region of Turkey due to its high adaptive abilities
combined with continuous growth and formation of
abundant leaf biomass (Yavuzsefik et al. 2001). The
combination between the deep root system and high
growth rate explain using of Paulownia plants for
bioremediation of polluted and degraded soils.
Our preliminary investigations with five selected
Paulownia hybrid lines (P. tomentosa 9 fortunei-TF,
P. elongata 9 fortunei-EF, P. elongata 9 for-
tunei 9 elongata-T2, P. elongata 9 elongata-T4, P.
elongata 9 kawakamii-EK), grown ex vitro as hydro-
ponic cultures at three levels of salinity—50, 100 and
200 mmol l-1 sodium chloride (NaCl) solution
123
Agroforest Syst
showed that TF and T4 lines are more salt resistant
because its net photosynthetic rate (PN) is enhanced,
whereas this parameter is reduced in T2 and EF
(Ivanova et al. 2014). The study of salinity effect on
in vitro and ex vitro growth of Paulownia species is
scarce (Ayala-Astorga and Alcaraz-Melendez 2010).
Elaborated on the system of suitable physiological
and biochemical markers will help to understand the
mechanisms of the salt resistance of Paulownia. The
differences in the distribution of Mg2?, Ca2?, Na?,
K? and Fe3? between water available soil fraction and
different organs of two hybrid Paulownia lines (P.
tomentosa 9 fortunei-TF and P. elongata 9 elon-
gata-T4), grown on two types of salinized soils during
two vegetative periods were investigated. The hypoth-
esis that both hybrid lines adapted any sort of
avoidance mechanisms towards increasing substrate
salinity is tested.
Materials and methods
Plant material
Four-year-old plantlets of Paulownia tomen-
tosa 9 fortunei-TF and Paulownia elongata 9 elon-
gata-T4, derived from in vitro micropropagation of
seedlings (Miladinova et al. 2013), were cultivated in
plastic pots with 2.5 kg soil, collected from two
different areas situated in the vicinity of the village
Belozem, Bulgaria. A sampling strategy was carried
out consisting of the collection of soil aliquots (about
10 kg) from the surface and at depths of 30–60 cm in
two different locations of the area. The soil samples
were combined (full weight about 60 kg), air dried and
sieved through nylon mesh and then mixed with sand
in the ratio 3:1. On the basis of agrochemical
characteristics the first type of soil was characterized
as non-saline and the second type of soil might be
determined as middle alkaline (Referative basic data
2009). The second saline soil possessed exchangeable
Na content about 5.3 times higher and Sodium
Adsorption Ratio about 6 times higher in comparison
with the first non-saline soil. The electrical conduc-
tivity were: saline soil—14.0 mS/cm, non-saline—6.3
mS/cm (Ivanova et al. 2015). The experiment was set
as 4 treatments, with 7 replications and was conducted
in a glasshouse (natural sunlight, temperatures
15–35 °C, relative humidity 40–65%) for two
Agroforest Syst
vegetation seasons. The pots were irrigated daily with
tap water to exceeding the field capacity of the soils.
Growth parameters
The plants were harvested to determine gravimetri-
cally plants dry mass (leaf, petiole, stem) after heating
at 60 °C. Leaf area (LA) was calculated using software
program SigmaScan Pro 5. The following indexes
were calculated: total leaf area/total dry mass (LAR),
total leaf area/leaf number (MLA).
Plant and soil metal analysis
The water soluble bioavailable fraction (free metal
ions, soluble metal complexes and metals adsorbed to
inorganic soil constituents at ion exchange sites—
Mg2?, Ca2?, Na?, K? and Fe3?) from the soils was
determined by extraction tests (Doumett et al. 2008).
Total metal content in available fractions and plant
organ samples was determined by atomic absorption
spectrophotometric analysis (Perkin-Elmer 5000,
UK), after acidic digestion with Suprapur grade Fluka
reagents.
Gas exchange measurements
Assimilation (A, lmol CO2 m-2 s-1) versus sub-
stomatal CO2 concentration (Ci, lmol mol-1)
response curve (A:Ci) of fully developed attached
leaves of P. tomentosa 9 fortunei and P. elon-
gata 9 elongata were measured for at least two
leaves using portable photosynthesis open system
(Li-6400; Licor Inc., Lincoln, Nebraska, USA). The
A:Ci response curve was generated after setting the
environment inside the leaf chamber: leaf-to-air vapor
pressure deficit was 1.5 kPa, leaf temperature was
20 °C, light saturation capacity 1000 lmol m-2 s-1
blue/red light (Li-6400-02-LED light source). CO2
regulator (Li-6400-01) provided different CO2 con-
centrations (Ca) in the range 1000–50 lmol/mol. The
A:Ci measurements started at a CO2 concentration
close to ambient (350 lmol/mol) and continued down
to 50 lmol/mol in a step-wise fashion, then up again to
1000 lmol/mol through the ambient CO2 concentra-
tion. At each step, gas exchange variables were
recorded after achieving steady-state conditions. Cal-
culations of gas exchange parameters were performed
according to Von Caemmerrer and Farquhar (1981).
Data of each A:Ci curve were fitted into a nonrectan-
gular hyperbola equation (Jones 1992). Mechanistic
analysis of each A:Ci curve was performed (Farquhar
et al. 1980). The model was used to estimate the
maximal Rubisco catalyzed carboxylation velocity
(Vcmax) and CO2 compensation point (C). The relative
contribution of stomatal limitation to photosynthesis,
maximal electron transport rate (Jmax), triose phos-
phate utilization rate (VTRU) and CO2 which was the
proportional decrease in light-saturated (A) attributed
to stomatal component (SL, %) was calculated (Far-
quhar and Sharkey 1982).
Statistical analysis
Data were expressed as mean ± SE, where n was
given into the tables. Comparison of means was
performed by the Fisher LSD test (P B 0.05) after
performing ANOVA analysis.
Results and discussion
Effect of soil salinity on the distribution of metals
The water bioavailable amount of target alkaline and
alkaline earth metals present in the fractions of the
soils before planting showed that Ca2? and Na?
prevailed in saline soil (Table 1). Higher Mg2?, Fe3?
and especially Na? and K? contents are established in
the fractions from the non-saline soil after harvesting
of both plants. The obtained ratio K?/Na? in these
fractions is reduced about 3 times after harvesting of
T4 (0.32) in comparison with TF (0.98). The pH values
decreased too from alkaline to middle acidic. The
accumulation of Na? and K? prevailed in the roots of
both hybrid lines grown on non-saline soil (Table 2).
The differences in the content of these elements in the
roots of both plants grown on saline soil are insignif-
icant. Nevertheless, the obtained ratio K?/Na? in T4 is
1.2 time higher (13.93) than that in TF (12.00). The
results showed that both hybrid plants grown on non-
saline soil avoid stress by excreting excess contents of
alkaline metals and Fe3? in the rhizosphere zone. The
strategy of salt exclusion relies on the selective release
of Na? into the xylem and its resorption from the
xylem stream. Net accumulation of the Na? in the
plants is dependent on the balance between passive
influx and active efflux. Salt exclusion operates at the
123
 Agroforest Syst

Table 1 Bioavailable alkaline, alkaline earth metal and Fe3? contents [mg/l] in non-saline and saline soils before planting and after
harvesting the plants
Soil type Mg2? Ca2? Na? K? Fe3? K?/Na? pH

Before planting
Non-saline 29.0 ± 2.5a 10.0 ± 1.3a 26.5 ± 2.9a 34.0 ± 2.9a 8.3 ± 0.9a 1.28 8.00
Saline 40.0 ± 3.5b 187.0 ± 12.3b 382.2 ± 24.9b 50.0 ± 4.9b 0.2 ± 0.05b 0.13 8.92
After harvesting of TF
Non-saline 45.0 ± 3.7a 0.7 ± 0.02a 178.2 ± 2.6a 174.0 ± 20.9a 495.0 ± 39.6a 0.98 5.66
Saline 40.0 ± 3.0b 28.6 ± 2.5b 53.2 ± 4.8b 42.0 ± 3.7b 40.2 ± 4.2 b 0.79 6.66
After harvesting of T4
Non-saline 22.0 ± 2.1a 3.2 ± 1.1a 338.8 ± 23.9b 110.0 ± 19.9a 220.3 ± 91.3a 0.32 5.82
Saline 27.0 ± 1.5b 41.8 ± 2.9b 78.1 ± 6.7b 29.0 ± 3.6b 27.0 ± 5.5 b 0.37 6.85
Notes Values are mean ± SE, n = 3; different letters indicate significant differences assessed by Fisher LSD test (P B 0.05) after
performing one-way ANOVA analysis

Table 2 Accumulation of alkaline, alkaline earth metal and Fe3? contents [mg/g DW] in the roots and shoot of TF and T4 hybrid
plants grown on non-saline and saline soil
Soil type Mg2? Ca2? Na? R? Fe3? R?/Na?

TF root
Non-saline 1.79 ± 0.7a 0.66 ± 0.05a 2.75 ± 0.8a 17.37 ± 2.1a 0.96 ± 0.06a 6.32
Saline 1.39 ± 0.2a 0.65 ± 0.03a 0.72 ± 0.06b 8.58 ± 0.7b 1.86 ± 0.20b 12.00
T4 root
Non-saline 2.92 ± 0.4a 0.85 ± 0.07a 3.37 ± 0.5a 14.85 ± 1.9a 2.79 ± 0.3a 4.41
Saline 2.23 ± 0.5a 1.08 ± 0.09a 0.74 ± 0.6b 10.27 ± 1.1b 2.14 ± 0.2b 13.93
TF shoot
Non-saline 2.94 ± 0.4a 6.06 ± 0.5a 0.071 ± 0.005a 9.13 ± 0.8a 0.133 ± 0.02a 128.59
Saline 1.87 ± 0.2b 6.51 ± 0.6a 0.072 ± 0.006a 9.90 ± 0.9a 0.158 ± 0.02b 137.50
T4 shoot
Non-saline 1.48 ± 0.2a 6.51 ± 0.6a 0.116 ± 0.02a 7.81 ± 0.6a 0.085 ± 0.007a 67.24
Saline 2.11 ± 0.2b 2.08 ± 0.2b 0.156 ± 0.06b 8.92 ± 0.8b 0.093 ± 0.008b 57.22
Notes Values are mean ± SE, n = 3; different letters indicate significant differences assessed by Fisher LSD test (P B 0.05) after
performing one-way ANOVA analysis

cellular and whole plant level (Munns et al. 1983) and
is to a great extent related to regulation of K?/Na?
selectivity (Jeschke and Hartung 2000). The salt
tolerance in species that exclude salts is achieved by
changes between Na? and Ca2?, rather than changes
in osmotic potential since adsorption of Ca2? on
membranes of root cells leads to reduced penetration
of monovalent cations (Munns et al. 1983). This is
demonstrated for wheat where inhibition of non-
directional Na? influx occurred following the addition
of external Ca2? (Reid and Smith 2000). Salt
exclusion is a very efficient but complex way of
preventing massive ion uptake in the root zone,
enabling a lower uptake and accumulation of salts in
the upper parts of the plant, especially in the transpir-
ing organs. Salt sensitive plants, such as beans and
maize are the most prominent Na? excluders (Jacoby
1994; Bayuelo-Jimenez et al. 2003). The accumula-
tion of Ca2? in the leaves of TF is 3 times higher than
that of T4 grown on non-saline and saline soils at the
end of the second vegetative season. Na? prevailed in
the leaves of T4 grown on both soils. The

123
Agroforest Syst

accumulation of Fe3? is more in the leaves of TF
(Table 3). Our results showed acropetal concentration
gradient of metals distribution between soil pore water
and plant tissues with the exception of Ca2?. The K?
accumulation in the fully developed leaves of both
lines is highest as compared to Na? at the end of
second vegetation season. Changes in K? and Na?
concentrations reflected in the K?/Na? ratio
(Table 2). This ratio is an important selection criterion
for salt tolerance (Ashraf and Orooj 2006). The K?/
Na? ratio decreased by increasing salt concentration
in safflower cultivars grown in hydroponics, but
highest values determined more tolerant to salt stress
plant species (Erdal and Çakirlar 2014). The obtained
ratio K?/Na? in T4 is twice lower in comparison with
TF has grown on non-saline and saline soils. Irrespec-
tive of salt exclusion by root membranes, leaf content
of K? and Na? remain similar as compared to plants
grown on saline soil (Table 2).
Effect of soil salinity on seedlings growth
The investigations showed that plant growth is limited
under salt stress (Maeda and Nakazawa 2008). TF
grown on non-saline soil formed higher fresh and dry
biomass, total leaf area and MLA ratio than those of
T4. The ratio root/shoot dry biomass is higher in T4 as
compared to TF. With increasing soil salinity the
enhancement of growth parameters of T4 (stem length,
leaf number, total dry biomass, total leaf area) is
observed in comparison with TF. Two important
parameters characterizing photosynthetic leaf
surface—LAR and MLA are enhanced in TF, while
in T4 grown on the saline soil it decreased insignif-
icantly. The ratio root/shoot dry biomass is enhanced
more in TF than in T4 (Table 3). Besides salt
exclusion in the roots, low NaCl levels in leaves can
also be achieved by salt retention in the lower plant
parts and also through abscission of old leaves once
they accumulate large quantities of salts. The mech-
anism of intra-plant allocation is also characteristic for
many halophytes, which, due to the limited transpira-
tion, can keep an excess of salts within their roots and
lower parts of the shoot, thus preventing ion accumu-
lation in the photosynthetic tissues (Dajic 2006). We
established yellowing and later abscission of older
leaves of both hybrid plants during vegetation. The
leaf abscission is observed mainly in TF grown on the
saline soil as compared to non-saline soil and can be
considered as avoidance mechanism by which is
preserved younger leaves from the action of high salt
concentrations.
Effect of soil salinity on seedlings photosynthetic
gas exchanges
The estimated Vcmax and Jmax on the base of (A:Ci)
curves were reduced in TF by 11 and 20%, respec-
tively. The same parameters increased in T4 by 20 and
14%, respectively. The value of VTPU declined in TF
by 5%, while in T4 increased by 15%, respectively.
The CO2 compensation point (C) is significantly
higher in TF, but in T4 decreased slightly. The SL
values are enhanced in both hybrid lines (Table 4).

Table 3 Changes in stem length, leaf number, total fresh mass mass (LAR) and ratio total leaf area/leaf number (MLA) in TF
(FW) and total dry mass (DW), ratio dry root/shoot mass and T4 hybrid plants grown on non-saline (1) and saline soil
(DWroot/shoot), total leaf area (LA), ratio total leaf area/total dry (2)
Lines TF(1) T4(1) TF(2) T4(2)

Stem length, cm 33.0 ± 2.5b 32.0 ± 2.7b 26.0 ± 1.8a 48.0 ± 3.6a
Leaf number 26 ± 1.9b 22 ± 1.5b 18 ± 1.1a 26 ± 1.7a
FW, g 48.642 ± 4.67b 27.156 ± 1.86b 62.713 ± 5.15a 40.177 ± 3.75a
DW, g 26.552 ± 2.622a 15.029 ± 1.544a 17.561 ± 1.618b 16.898 ± 1.543a
DWroot/shoot 0.471 0.541 1.010 0.752
2
LA, cm 823.56 ± 78.42a 655.93 ± 52.48b 731.68 ± 68.26b 720.12 ± 66.64a
LAR, cm2/g 31.02 ± 2.69b 43.64 ± 3.18a 41.66 ± 3.87a 42.62 ± 3.27a
MLA 31.67 ± 1.92b 29.82 ± 1.78a 40.64 ± 3.46a 27.70 ± 1.86b
Notes Values are mean ± SE, n = 7; different letters indicate significant differences assessed by Fisher LSD test (P B 0.05) after
performing one-way ANOVA analysis

123

Table 4 Photosynthetic gas exchange parameters derived from the (A:Ci) response curves of TF and T4 hybrid plants grown on non-
saline (1) and saline soil (2)
Lines Vc max Jmax
TF1 49.35 ± 3.23a 50.88 ± 4.09a
T41 45.90 ± 4.35a 49.19 ± 5.67a
TF2 43.69 ± 3.37b 40.59 ± 3.55b
T42 55.26 ± 5.21b 56.14 ± 2.69b
Notes Values are means of at least three replicates per treatment. Different letters indicate significant differences assessed by Fisher
LSD test (P B 0.05) after performing one-way ANOVA analysis. Variables are: maximal Rubisco catalyzed carboxylation velocity—
Vcmax (lmol CO2/(m2 s)); maximal electron transport rate—Jmax (lmol electron/(m2 s)); triose phosphate utilization rate—VTPU
(lmol CO2/(m2 s)); CO2 compensation point—C (lmol/mol); stomatal limitation to photosynthesis—SL (%)
Salinity reduced net-photosynthesis (PN) and stomatal
conductivity (Gs) in most plant species (Munns and
Tester 2008). The results showed that balance between
water loss and CO2 uptake helps to find a weak spot in
the mechanism of adjustment of photosynthesis to
high salinity. Biomass production of plants depended
mainly on the ability to keep a high net-photosynthe-
sis, minimum transpiration, low stomatal conductiv-
ity, and minimum internal CO2 concentration at their
threshold salinity tolerance. Analysis of (A:Ci) curves
indicated that only in the leaves of TF, salinity induced
decline in the carboxylation efficiency of Rubisco
enzyme, reduced the rate of electron supply by the
electron transport system for ribulose-1,5-bisphos-
phate regeneration and limited the available inorganic
phosphorus for Calvin cycle (expressed by the
decrease in Vcmax, Jmax, and VTPU). CO2 compensa-
tion point (C) increased in TF by 25%, while in T4
decreased by 13%, respectively (Table 4). The values
for SL increased more significantly in TF than in T4
under salinity (Table 4). That is why the reduction of
net-photosynthesis is attributed to both stomatal
closures and to the biochemical components of the
photosynthetic process. Under saline conditions, the
stomatal component played a more dominant role over
biochemical components in limiting the photosyn-
thetic gas exchange. Our preliminary results showed
that PN, Gs and WUE are more reduced in TF than in
T4 grown on saline soil, while transpiration is
enhanced insignificantly (Ivanova et al. 2015).
Declined stomatal conductance may provide a down
regulatory mechanism for controlling salt loading in
plants with limited salt compartment capacities
(Robinson et al. 1997). The established morphologi-
cal, biochemical and stomatal responses to salinity are
123
Agroforest Syst
VTPU C SL
7.99 ± 0.73a 58.25 ± 4.45a 19.23 ± 1.14a
7.59 ± 0.65a 69.23 ± 5.67a 18.18 ± 1.99a
7.61 ± 0.78a 72.72 ± 0.76b 27.78 ± 1.65b
8.77 ± 0.96b 60.00 ± 5.62b 22.94 ± 1.89a
more pronounced in TF than in T4 and have
contributed to the overall reduction in carbon gain
and then a reduction in plant growth.
In conclusion, determination of the Paulownia
hybrid lines responses to soil salinity and development
of more tolerant line is important. The results of this
study showed that salt stress more negatively affected
growth and photosynthetic gas exchange in TF than in
T4. The counted parameters may be used as reliable
indicators for the investigation tolerance mechanisms
in these lines.
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